Julius S. Lipp

The growing research into the archaeal lipidome has uncovered a remarkable structural diversity in isoprenoidal glycerol dialkyl glycerol tetraethers (iGDGTs) and revealed complex membrane adaptations, especially in extreme environments. We performed a comprehensive analysis of the lipidome from the subsurface aquifer of the CO ₂ ‐rich, cold‐water Geyser Andernach (Germany), using ultra‐high‐resolution mass spectrometry. We detected iGDGT‐0, presumably derived from the dominant community member Candidatus Altiarchaeum, providing supporting evidence for its ability to synthesise tetraethers, as previously predicted from metagenomic data. Beyond the typical iGDGT‐0 and acyclic glycerol trialkyl glycerol tetraether (iGTGT‐0), we discovered novel structural derivatives, here referred to as extended iGDGTs and iGTGTs, characterised by the asymmetrical addition of up to two isoprenoid units to only one of their hydrocarbon side chains, analogous to those found in extended archaeols. The apparent absence of GDGT ring synthase A and B genes in the corresponding metagenome‐assembled genome raises the possibility that the producing archaea may utilise extended iGDGTs as a membrane adaptation to cope with the nutrient‐depleted conditions of the geyser environment, highlighting the adaptive flexibility of archaea to extreme physicochemical conditions.

The Paleocene–Eocene Thermal Maximum (PETM; 55.9 million years ago) was a rapid, CO2-driven climate polycrisis, with global warming of 5-6°C1,2, ocean acidification3-5, and deoxygenation6-8. These stresses may have affected marine nitrogen cycling, particularly nitrification—a major source of nitrous oxide (N2O) 9 that remains underexplored on geological timescales. By integrating proxy records with Earth System modeling, we show that nitrification globally increased by ~56% during the PETM. Inhibiting effects of ocean deoxygenation10 and acidification11 on nitrification were outweighed by increased ammonium supply and nitrifier niche expansion. Enhanced nitrification led to a ~290% increase in total marine N2O production, contributing 0.3-1.4℃ of warming during the PETM. Our results highlight a strong, positive climatic feedback from nitrogen cycle perturbations under extreme global warming, ocean deoxygenation and acidification.

The growing research into the archaeal lipidome has uncovered a remarkable structural diversity in glycerol dialkyl glycerol tetraethers (GDGTs) and revealed complex membrane adaptations, especially in extreme environments. We performed a comprehensive analysis of the lipidome from the subsurface water of a CO ₂ -rich, cold-water Geyser Andernach (Germany), using ultra-high-resolution mass spectrometry methods. We detected GDGT-0, presumably derived from the dominant community member Candidatus Altiarchaeum, providing evidence for its ability to synthesize tetraethers as previously predicted from metagenomic data. Beyond the typical GDGT-0 and acyclic glycerol trialkyl glycerol tetraether (GTGT-0), we discovered novel structural analogues, here referred to as extended GDGTs and GTGTs, characterized by the asymmetrical addition of up to two isoprenoid units to only one of their hydrocarbon side chains, analogous to those found in extended archaeols. The lack of GDGT ring synthase A (GrsA) and GrsB homologs in the corresponding metagenome-assembled genome, suggests that the producing archaeon may utilize extended GDGTs as a membrane adaptation to cope with the energy-depleted conditions of the geyser environment, highlighting the adaptive flexibility of archaea to extreme physicochemical conditions.

Microbial responses to environmental changes are well studied in laboratory cultures, but in situ adaptations of plankton lipidomes remain less understood. Building upon a global lipidomic study showing temperature-driven lipid unsaturation regulation in marine plankton, we expanded the analysis spatially and methodologically to investigate the in situ adaptations of marine plankton. Through weighted correlation network analysis of 3164 lipid species from 930 samples, we identified 16 structurally distinct lipid clusters co-occurred across diverse oceanographic conditions. The highest lipid diversity was observed in the polar oceans, where plankton uses chain shortening for cold acclimation. Conversely, in the surface of tropical and subtropical oceans, plankton showed enrichment in non-phosphorus lipids, likely responding to warm temperature, with potential implications for the elemental stoichiometry of the biological pump. In the subsurface of these regions, highly unsaturated lipids were enriched, suggesting phytoplankton adaptation to low light and contributing unsaturated fatty acids to tropical and subtropical ocean food webs.

A recent global survey of planktonic lipids showed a fundamental temperature-mediated regulation of lipid unsaturation in the global oceans [Holm H, et al. (2022) Science 376:1487–1491]. We expand the analysis of this dataset, both spatially and methodologically, to examine diverse environmental stressors across the ocean. Utilizing weighted correlation network analysis, we analyzed 3,164 lipid features in the dataset comprising 930 samples of suspended particulate matter, taken across a broad range of oceanographic conditions and water depths up to 600 meters. A total of 16 lipid clusters being co-expressed across diverse environments were identified. This analysis reveals universal relationships between environmental factors and the lipidome of the planktonic community. The largest lipid cluster, comprising 481 lipid features, including glycerolipids with polyunsaturated fatty acids, exhibited a significant enrichment in polar oceans, suggesting the highest lipid diversity in these ocean regions. Remarkably, marine plankton in these regions employ both desaturation and chain shortening for cold acclimation. Additionally, one lipid cluster strongly linked to the plankton residing in the surface of tropical and subtropical oceans was enriched with non-phosphorus lipids. We suggest this adaptive response enables the plankton to cope with phosphorous scarcity and heat stress. Notably, in the subsurface of these regions, a co-expressed cluster of highly unsaturated lipids is consistent with an enhanced production of polyunsaturated fatty acids by phytoplankton, possibly for low light adaptation. This adaptation is important as it may represent a source of essential fatty acids below the warm sea surface where such vital compounds may be diminished in the warmer future. Significance Marine plankton is vital for marine ecosystems and climate regulation. We analyzed a large lipidomics dataset of 930 samples collected from global oceans. This allowed us to explore how plankton adapt their lipidomes across different environments. Our findings show distinct lipid clusters correlating with specific environmental conditions, revealing mechanisms like chain shortening to cope with cold stress, enrichment of non-phosphorus lipids in tropical surface waters, and increased polyunsaturated fatty acids in low-light tropical subsurface areas. These adaptations are crucial for understanding how climate change will impact marine ecosystems.

The Black Sea is a permanently anoxic, marine basin serving as model system for the deposition of organic‐rich sediments in a highly stratified ocean. In such systems, archaeal lipids are widely used as paleoceanographic and biogeochemical proxies; however, the diverse planktonic and benthic sources as well as their potentially distinct diagenetic fate may complicate their application. To track the flux of archaeal lipids and to constrain their sources and turnover, we quantitatively examined the distributions and stable carbon isotopic compositions (δ¹³C) of intact polar lipids (IPLs) and core lipids (CLs) from the upper oxic water column into the underlying sediments, reaching deposits from the last glacial. The distribution of IPLs responded more sensitively to the geochemical zonation than the CLs, with the latter being governed by the deposition from the chemocline. The isotopic composition of archaeal lipids indicates CLs and IPLs in the deep anoxic water column have negligible influence on the sedimentary pool. Archaeol substitutes tetraether lipids as the most abundant IPL in the deep anoxic water column and the lacustrine methanic zone. Its elevated IPL/CL ratios and negative δ¹³C values indicate active methane metabolism. Sedimentary CL‐ and IPL‐crenarchaeol were exclusively derived from the water column, as indicated by non‐variable δ¹³C values that are identical to those in the chemocline and by the low BIT (branched isoprenoid tetraether index). By contrast, in situ production accounts on average for 22% of the sedimentary IPL‐GDGT‐0 (glycerol dibiphytanyl glycerol tetraether) based on isotopic mass balance using the fermentation product lactate as an endmember for the dissolved substrate pool. Despite the structural similarity, glycosidic crenarchaeol appears to be more recalcitrant in comparison to its non‐cycloalkylated counterpart GDGT‐0, as indicated by its consistently higher IPL/CL ratio in sediments. The higher TEX₈₆, CCaT, and GDGT‐2/‐3 values in glacial sediments could plausibly result from selective turnover of archaeal lipids and/or an archaeal ecology shift during the transition from the glacial lacustrine to the Holocene marine setting. Our in‐depth molecular‐isotopic examination of archaeal core and intact polar lipids provided new constraints on the sources and fate of archaeal lipids and their applicability in paleoceanographic and biogeochemical studies.

Methanogenic and methanotrophic archaea produce and consume the greenhouse gas methane, respectively, using the reversible enzyme methyl-coenzyme M reductase (Mcr). Recently, Mcr variants that can activate multicarbon alkanes have been recovered from archaeal enrichment cultures. These enzymes, called alkyl-coenzyme M reductase (Acrs), are widespread in the environment but remain poorly understood. Here we produced anoxic cultures degrading mid-chain petroleum n-alkanes between pentane (C₅) and tetradecane (C₁₄) at 70 °C using oil-rich Guaymas Basin sediments. In these cultures, archaea of the genus Candidatus Alkanophaga activate the alkanes with Acrs and completely oxidize the alkyl groups to CO₂. Ca. Alkanophaga form a deep-branching sister clade to the methanotrophs ANME-1 and are closely related to the short-chain alkane oxidizers Ca. Syntrophoarchaeum. Incapable of sulfate reduction, Ca. Alkanophaga shuttle electrons released from alkane oxidation to the sulfate-reducing Ca. Thermodesulfobacterium syntrophicum. These syntrophic consortia are potential key players in petroleum degradation in heated oil reservoirs.

As a hallmark of Archaea, their cell membranes are comprised of ether lipids. However, Archaea‐type ether lipids have recently been identified in Bacteria as well, with a somewhat different composition: In Bacillales, sn‐glycerol 1‐phosphate is etherified with one C35 isoprenoid chain, which is longer than the typical C20 chain in Archaea, and instead of a second isoprenoid chain, the product heptaprenylglyceryl phosphate becomes dephosphorylated and afterward diacetylated by the O‐acetyltransferase YvoF. Interestingly, database searches have revealed YvoF homologs in Halobacteria (Archaea), too. Here, we demonstrate that YvoF from Haloferax volcanii can acetylate geranylgeranylglycerol in vitro. Additionally, we present the first‐time identification of acetylated diether lipids in H. volcanii and Halobacterium salinarum by mass spectrometry. A variety of different acetylated lipids, namely acetylated archaeol, and acetylated archaetidylglycerol, were found, suggesting that halobacterial YvoF has a broad substrate range. We suppose that the acetyl group might serve to modify the polarity of the lipid headgroup, with still unknown biological effects.

Butanetriol and pentanetriol dibiphytanyl glycerol tetraethers are membrane lipids recently discovered in anoxic environments. These lipids differ from typical membrane-spanning tetraether lipids because they possess a nonglycerol backbone.

Varved sediments from the center of the Santa Barbara Basin (SBB) off southern California are a valuable archive for high‐resolution climate reconstruction. Using mass spectrometry imaging of lipid biomarkers, this study examines interactions of perennial upwelling strength and oxygen‐driven redox conditions at the sediment‐water interface from 1900 CE to 2009. In the SBB, variations in upwelling are recorded by isoprenoidal tetraethers from planktonic archaea, while the redox‐sensitive C₂₉ stanol/stenol ratio reflects oxygen content in the bottom water and surficial sediment. The changing coherence of these two proxies allows investigation of the interplay between upwelling, bioproductivity and redox conditions, and their dependence on SBB source water composition during the 20th century. Prior to a large‐scale oceanographic regime shift observed in the North Pacific in the 1970s, both proxies are positively correlated: periods of enhanced upwelling promoted mixing, resulting in increased oxygen availability at the sediment‐water interface; conversely periods of reduced upwelling favored development of oxygen‐depleted water at depth. In the wake of the basin‐wide regime shift, changing oceanographic conditions led to a reduction in the southward flowing California Current and a stronger influence of the poleward California Undercurrent, which increased stratification and the supply of warm, oxygen‐poor tropical water in the subsurface. As a result, oxygen availability in SBB bottom waters was predominantly regulated by upwelling‐induced productivity and subsequent oxygen‐consuming remineralization of organic matter.